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of pressure and temperature alone limit Rona et al., Eds. (Plenum, New York, 1983), 19. A. Williams, Proc. Biol. Soc. Wash. 93, 443 pp. 735-770. (1980). the activities of deep-sea organisms. 3. Galapagos Biology Expedition Participants, 20. P. Pugh, Philos. Trans. R. Soc. London 301, 165 Microorganisms and the food chains that Oceanus 22, 1 (1979); K. Crane and R. Ballard, (1983); K. Woodwick and T. Sensenbaugh, J. Geophys. Res. 85, 1443 (1980); J. F. Grassle Proc. Biol. Soc. Wash., in press. depend on them have evolved in re- in Hydrothermal Processes at Seafloor Spread- 21. RISE Project Group, Science 207, 1421 (1980); ing Centers, P. A. Rona et al., Eds. (Plenum, F. Gaill et al., C. R. Acad. Sci. 298, 553 (1984); sponse to the rich supply of reduced New York, 1983), pp. 665-676. ibid., p. 331. compounds available for chemosynthe- 4. D. Desbruyeres, P. Crassous, J. Grassle, A. 22. D. Cohen and R. Haedrich, Deep-Sea Res. 30, Khripounoff, D. Reyes, M. Rio, M. Van Praet, 371 (1983). sis. A further constraint is that the ani- C. R. Acad. Sci. 295, 489 (1982). 23. R. Lutz, L. Fritz, D. Rhoads, Eos 64, 1017 mals must continually colonize new 5. R. Ballard, J. Francheteau, T. Juteau, C. Ran- (1983). gan, W. Normark, Earth Planet. Sci. Lett. 55, 1 24. K. Macdonald et al., Earth Planet. Sci. Lett. 48, vents tens and occasionally hundreds of (1981); R. Ballard, T. H. van Andel, R. Hol- 1 (1980). kilometers away. Despite differences in comb, J. Geophys. Res. 87, 1149 (1982); R. 25. K. Turekian, J. K. Cochran, Y. Nozaki, Nature Ballard, R. Hekinian, J. Francheteau, Earth (London) 280, 385 (1979); K. K. Turekian and J. faunal composition and at least partial Planet. Sci. Lett. 69, 176 (1984). K. Cochran, Science 214, 909 (1981); , J. 6. L. Laubier and D. Desbruyeres, La Recherche Bennett, Nature (London) 303, 55 (1983). isolation of vent fields, these communi- 161, 1506 (1984). 26. C. Berg, Bull. Biol. Soc. Wash., in press. ties have had a long evolutionary his- 7. R. Turner and R. Lutz, Oceanus 27, 54 (1984); 27. Observations made by K. Turekian. Florida Escarpment Cruise Participants, ibid., 28. K. Turekian et al., Proc. Natl. Acad. Sci. tory. Fossil vent worm tubes have been p. 32. U.S.A. 72, 2829 (1975). identified in Cretaceous sulfide ores (34), 8. J. Grassle, personal communication. 29. J. F. Grassle and L. Morse-Porteous, unpub- 9. J. McLean, Bull. Biol. Soc. Wash., in press. lished data; H. Sanders and J. Allen, Bull. Mus. and the nearest relative of the archeogas- 10. M. Jones, Oceanus 27, 47 (1984). Comp. Zool. Harv. Univ. 145, 237 (1973). tropod limpets date from the Paleozoic, 11. D. Desbruyeres and L. Laubier, Oceanol. Acta 30. R. D. Turner, Science 180, 1377 (1973). 3, 267 (1980); Proc. Biol. Soc. Wash. 95, 484 31. , personal communication. over 200 million years ago (9). The co- (1982); V. Tunnicliffe, Eos 64, 1017 (1983); per- 32. H. Jannasch and C. Taylor, Annu. Rev. Micro- sonal communication. biol. 38, 487 (1984). occurrence of a clam, a mussel, and a 12. J. F. Grassle et al., Bull. Biol. Soc. Wash., in 33. J. Childress and T. Mickel, Eos 64, 1018 (1983); vestimentiferan worm at widely separat- press. J. Childress and R. Mickel, Mar. Biol. Lett. 3, 13. J. Enright et al., Nature (London) 289, 219 73 (1982); T. Mickel and J. Childress, Biol. Bull. ed sites in the Pacific and Atlantic repre- (1981); P. Lonsdale, Deep-Sea Res. 24, 857 (Woods Hole, Mass.) 162, 70 (1982). sents either an unusual distribution from (1977). 34. R. M. Haymon, R. A. Koski, C. Sinclair, Sci- 14. C. M. Cavanaugh et al., Science 213, 340 (1981); ence 223, 1407 (1984). a single lineage or, even more remark- Nature (London) 302, 58 (1983); H. Felbeck, 35. I thank the crew of DSRV Alvin and S. Brown- ably, cases of parallel evolution. Science 213, 336 (1981); Nature (London) 293, Leger, L. Morse-Porteous, R. Petrecca, and I. 291 (1981). Williams for technical assistance; I thank J. P. 15. P. Comita and R. Gagosian, Nature (London) Grassle, L. Morse-Porteous, and J. M. Peterson References and Notes 307, 450 (1984). for invaluable comments and assistance in the 16. K. L. Smith, Ecology 66, 1067 (1985). preparation of the manuscript. The work was 1. J. Brooks et al., Eos 66, 106 (1985); Canadian 17. G. H. Rau, Nature (London) 289, 484 (1981); supported by grants OCE7810458, OCE7810459, American Seamount Expedition, Nature (Lon- and J. I. Hedges, Science 203, 648 OCE8115251, and OCE8311201 from the Na- don) 313, 212 (1985); C. Paull et al., Science 226, (1979); G. H. Rau, ibid. 213, 338 (1981); B. Fry, tional Science Foundation. This is contribution 965 (1984). H. Gest, J. Hayes, Nature (London) 306, 51 No. 5963 of the Woods Hole Oceanographic 2. R. Hessler and W. Smithey, in Hydrothermal (1983). Institution, 71 of the GaI.pagos Rift Biology Processes at Seafloor Spreading Centers, P. A. 18. D. Rhoads et al., J. Mar. Res. 40, 503 (1982). Expedition, and 50 of the Oasis Expedition. eukaryotic organisms. At the same time, bacteria retain a much wider metabolic diversity than is found in plants and animals. Because of the resulting bio- chemical versatility of natural microbial Geomicrobiology of Deep-Sea populations and the smallness, general resistance, and dispersibility of bacterial Hydrothermal Vents cells, these organisms are able to exist in more extreme environments than the higher organisms. Therefore, the occur- Holger W. Jannasch and Michael J. Mottl rence of certain microorganisms at deep- sea vents was predictable; however, their ability to make it possible for higher forms of life to thrive with an unusual Deep-sea hydrothermal vents were tures of 2700 to 380°C and flow rates of 1 efficiency on inorganic sources of energy discovered in the 1970's after an exten- to 2 m sec'1. Hot vent fields commonly in the absence of light was entirely unex- sive search along the GalApagos Rift (1, include warm- and intermediate-tem- pected. 2), a part of the globe-encircling system perature vents (0300TC) ("white smok- of sea-floor spreading axes. During the ers") as well as high-temperature vents past 7 years, more hydrothermal vent (3500 ± 20C) ("black smokers"). A high- Chemosynthesis fields have been located along the East ly efficient microbial utilization of geo- Pacific Rise. They fall into two main thermal energy is apparent at these The most significant microbial process groups: (i) warm vent fields with maxi- sites-rich animal populations were taking place at the deep-sea vents is mum exit temperatures of 50 to 23°C and found to be clustered around these vents "bacterial chemosynthesis." The term flow rates of0.5 to 2 cm sec'1 and (ii) hot in the virtual absence of a photosynthetic was coined by Pfeffer in 1897 (6) in vent fields with maximum exit tempera- food source (3-5). obvious contrast to the then well-known Microorganisms, mainly bacteria, are photosynthesis. Both processes involve efficient geochemical agents. As pro- the of carbon com- Holger W. Jannasch is a senior scientist in the biosynthesis organic Biology Department and Michael J. Mottl, is an karyotic organisms, they lack a mem- pounds from C02, with the sour'ce of associate scientist in the Chemistry Department at Woods Hole Oceanographic Institution, Woods brane-bound nucleus and thereby the energy being either chemical oxidations Hole, Massachusetts 02543. complex genetic apparatus of the higher, or light, respectively. More specifically, i2 AUGUST 1985 717 Table 1. Electron sources and types of chemolithotrophic bacteria potentially occurring at the crust is responsible for the wide hydrothermal vents. range of exit temperatures (2, 10). Thus, chemical species that are nonreactive Electron donor Electron Organisms during mixing define mixing lines as a function of temperature for the warm S2-, SO, S2032 02 Sulfur-oxidizing bacteria S2-, 2 N03- Denitrifying and sulfur-oxidizing bacteria vent waters. These lines pass through SO, S203 ambient seawater and extrapolate to a H2 02 Hydrogen-oxidizing bacteria at 350°C similar to that actu- H2 NO3- Denitrifying hydrogen bacteria composition H2 S, S042- Sulfur- and sulfate-reducing bacteria ally measured in the hot vent waters. H2 CO2 Methanogenic and Most of the chemical species thought acetogenic bacteria in NH4+, N02 02 Nitrifying bacteria to participate microbiological reac- Fe2+, (Mn2+) 02 Iron- and manganese-oxidizing bacteria tions do not exhibit such linear mixing CH4, CO 02 Methylotrophic and carbon monoxide- behavior. These species may therefore oxidizing bacteria originate either at depth in the high- temperature end-member solution that has been produced by reaction of heated seawater with crustal rocks (11), or they chemoautotrophy refers to the assimila- bolic mechanism required for generating may originate in the shallow subsea-floor tion of CO2 and is coupled in some the necessary negative redox potential. region, either directly from bottom sea- bacteria to chemolithotrophy, the ability Some organisms have the ability to use water or as a result of various inorganic to use certain reduced inorganic com- organic compounds simultaneously as and organic reactions that occur on mix- pounds as energy sources. electron sources (mixotrophy). Since in ing (Fig. 1). In the present-day terminology, the autotrophy carbon (CO2) must be re- The concentrations of relevant species relation between photosynthetic and duced from a higher oxidative state than from the best-studied hot vent fields chemosynthetic metabolism is illustrated organic carbon, more energy is required (those on the East Pacific Rise near in the following schematic equations, than in heterotrophy. Therefore, obligate 21°N) and warm vent fields (those on the where the reduced carbon is represented chemoautotrophic bacteria generally Galapagos Rift near 86°W) are shown in as a carbohydrate, [CH2O]: grow more slowly than heterotrophs or Table 2.
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  • Primary Productivity Below the Seafloor at Deep-Sea Hot Springs

    Primary Productivity Below the Seafloor at Deep-Sea Hot Springs

    Primary productivity below the seafloor at deep-sea hot springs Jesse McNichola,1,2, Hryhoriy Stryhanyukb, Sean P. Sylvac, François Thomasa,3, Niculina Musatb, Jeffrey S. Seewaldc, and Stefan M. Sieverta,1 aBiology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543; bDepartment of Isotope Biogeochemistry, Helmholtz Centre for Environmental Research – Umweltforschungszentrum (UFZ), 04318 Leipzig, Germany; and cMarine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543 Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved May 16, 2018 (received for review March 13, 2018) Below the seafloor at deep-sea hot springs, mixing of geothermal but only one such measurement has been previously obtained under fluids with seawater supports a potentially vast microbial ecosys- realistic temperature and pressure conditions (4). Another im- tem. Although the identity of subseafloor microorganisms is largely portant consideration is that electron acceptors such as oxygen and known, their effect on deep-ocean biogeochemical cycles cannot nitrate rapidly become limiting during incubation experiments with be predicted without quantitative measurements of their meta- vent fluids (13, 14), which may lead to carbon fixation rates being bolic rates and growth efficiency. Here, we report on incubations greatly underestimated (13). However, it is difficult to ascertain the of subseafloor fluids under in situ conditions that quantitatively extent of this bias for existing studies because electron acceptor constrain subseafloor primary productivity, biomass standing stock, consumption has not typically been measured alongside carbon and turnover time. Single-cell-based activity measurements and 16S fixation. Theoretical estimates of primary productivity have also rRNA-gene analysis showed that Campylobacteria dominated car- been derived by combining geochemical measurements with ther- bon fixation and that oxygen concentration and temperature drove modynamic models (15, 16).